Infertility and fecundity loss of Wolbachia-infected Aedes aegypti hatched from quiescent eggs is expected to alter invasion dynamics

Abstract

The endosymbiotic bacterium Wolbachia shows viral blocking in its mosquito host, leading to its use in arboviral disease control. Releases with Wolbachia strains wMel and wAlbB infecting Aedes aegypti have taken place in several countries. Mosquito egg survival is a key factor influencing population persistence and this trait is also important when eggs are stored prior to releases. We therefore tested the viability of mosquitoes derived from Wolbachia wMel and wAlbB-infected as well as uninfected eggs after long-term storage under diurnal temperature cycles of 11–19°C and 22–30°C. Eggs stored at 11–19°C had higher hatch proportions than those stored at 22–30°C. Adult Wolbachia density declined when they emerged from eggs stored for longer, which was associated with incomplete cytoplasmic incompatibility (CI) when wMel-infected males were crossed with uninfected females. Females from stored eggs at both temperatures continued to show perfect maternal transmission of Wolbachia, but storage reduced the fecundity of both wMel and wAlbB-infected females relative to uninfected mosquitoes. Furthermore, we found a very strong negative impact of the wAlbB infection on the fertility of females stored at 22–30°C, with almost 80% of females hatching after 11 weeks of storage being infertile. Our findings provide guidance for storing Wolbachia-infected A. aegypti eggs to ensure high fitness adult mosquitoes for release. Importantly, they also highlight the likely impact of egg quiescence on the population dynamics of Wolbachia-infected populations in the field, and the potential for Wolbachia to suppress mosquito populations through cumulative fitness costs across warm and dry periods, with expected effects on dengue transmission.

Prevalence and molecular characterization of Wolbachia in field-collected Aedes albopictus, Anopheles sinensis, Armigeres subalbatus, Culex pipiens and Cx. tritaeniorhynchus in China

“…pipiens in July (P<0.01), in both females and males. Previous studies have indicated that the rearing temperature have significant effects on the fertility, frequency and density of mosquitoes and other arthropods infected with Wolbachia, especially wMel and wAlbB [42][43][44][45][46][47]. Further studies are needed to determine the effect on the infection of Wolbachia at more extreme temperature conditions (Table 3).…”

Temperature effects on cellular host-microbe interactions explain continent-wide endosymbiont prevalence

“…The fact that recently differentiated clinal wMel variants ($2,200 years ago) differ dramatically in oocyte abundance suggests that Wolbachiabased biocontrol programs should strategically leverage locally selected wMel variants, especially given that wMel is sensitive to temperature stress in mosquitoes. 83,[85][86][87][88] Temperature has emerged as an important mediator of Wolbachia-host interactions, 3,4,60,62,70,[89][90][91][92][93] and more broadly, temperature plays an influential role in the ecology and evolution of host-microbe associations. 22,94,95 As a consequence, rapidly changing environments are likely to influence Wolbachia prevalence in natural systems and the efficacy of Wolbachia-based biocontrol in vector systems.…”

Releasing incompatible males drives strong suppression across populations of wild and Wolbachia -carrying Aedes aegypti in Australia

“…aegypti exhibiting bidirectional incompatibility could provide an effective means of removing strains that accidently established in a landscape. However, the lower fitness of these Wolbachia females compared to the wild females already in the landscape ( 48 )—along with their potential deficiencies such as insecticide resistance common in many field populations ( 49 )—may permit some female leakage through the system early in releases; this would need to be reduced when a niche starts to empty ( 50 ). Alternatively, rotating Ae.…”